Systematic Prey Preference by Introduced Mice Exhausts the Ecosystem on Antipodes Island

Biol Invasions (2020) 22:1265–1278

https://doi.org/10.1007/s10530-019-02194-4 (0123456789().,-volV)( 0123456789().,-volV)

ORIGINAL PAPER

Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island

James C. Russell . Joanne E. Peace . Melissa J. Houghton . Sarah J. Bury . Thomas W. Bodey

Received: 5 August 2018 / Accepted: 10 December 2019 / Published online: 14 January 2020 Ó The Author(s) 2020

Abstract House mice (Mus musculus) are a wide- neighbouring mouse-free offshore islands together spread invasive species on islands. Where they are the with mouse stomach contents and stable isotope sole introduced mammal they can have particularly analyses of mouse livers to examine dietary prefer- strong negative impacts on recipient ecosystems. ences. We identified directly impacted and consumed House mice impacts have been documented on almost invertebrate Orders relative to their abundance and every component of the terrestrial ecosystem on provided a comprehensive picture of resource flow and Southern Ocean islands, including plants, inverte- overlap in the invaded terrestrial ecosystem. The brates, birds and ecosystem function. We undertook a remote terrestrial ecosystem of Antipodes Island was comprehensive study to determine the impacts of tightly circumscribed with strong resource overlap. house mice on Antipodes Island, New Zealand. This Mouse diet varied seasonally with resource availabil- study was done prior to mouse eradication to inform ity, dominated by invertebrates and land birds in monitoring and restoration. We used invertebrate summer, and plants and seabirds in winter. Inverte- pitfall trapping on the main Antipodes Island and brates that were preferentially preyed upon were Amphipoda, Lepidoptera and some species of Coleop- tera. These patterns suggest the ecosystem is annually J. C. Russell (&) Á J. E. Peace Á T. W. Bodey (&) School of Biological Sciences, University of Auckland, driven by a seasonal bottom-up resource pulse over Auckland 1142, New Zealand summer, where mice are a selective predator, differ- e-mail: [email protected] entially preying on invertebrates relative to inverte- T. W. Bodey brate abundance. Mice appear to be exhausting e-mail: [email protected] preferred prey as they systematically consume their way through the terrestrial ecosystem. Land bird M. J. Houghton Centre for Biodiversity and Conservation Science, School diet also varied seasonally and some of these birds of Biological Sciences, The University of Queensland, likely competed with mice for invertebrate prey. St. Lucia, QLD 4072, Australia Eradication of mice from Antipodes Island should reduce the predation on invertebrates and reduce the S. J. Bury National Institute of Water and Atmospheric Research effects of competition and predation on land birds. Ltd., Greta Point, Hataitai, Wellington 6021, New This should have flow-on effects to the abundance of Zealand invertebrates and endemic land bird sub-species of pipit and snipe. T. W. Bodey Environment and Sustainability Institute, University of Exeter, Penryn TR10 9FE, UK 123 1266 J. C. Russell et al.

Keywords Diet Á House mouse Á Mus musculus Á The Antipodes Islands exhibit high levels of Southern Ocean Á Invertebrates Á Stable isotopes Á invertebrate endemism (Marris 2000). There are 23 Stomach content native Coleoptera species with nine island endemics (Marris 2000) and 19 Lepidoptera species with four island endemics (Patrick 1994). The main Antipodes Island lacks medium-sized ﬂightless invertebrates, Introduction and mice have been invoked as the reason (Patrick 1994). For example, an undescribed weta species House mice (Mus musculus) are a widespread invasive (Orthoptera) is known from mouse-free offshore species and one of the most commonly introduced Bollons Island, but has not been collected from the rodent species to islands (Moors and Atkinson 1984; main Antipodes Island (Marris 2000; McIntosh 2001). Angel et al. 2009). They are hardy and adaptive with Investigations by Marris (2000) and Russell (2012) plastic dietary requirements allowing them to suc- inferred that mice impacted on the abundance, com- cessfully adapt to and establish themselves in a variety position, and distribution of the invertebrate fauna on of habitats (e.g. Renaud et al. 2015). Ecosystems Antipodes Island, but these investigations did not invaded by mice suffer various impacts, from seed directly study mouse diet. predation to attack of seabirds (Angel et al. 2009;St In this study, we initiated investigations to further Clair 2011; Bolton et al. 2014; Cuthbert et al. 2016), to clarify the impacts of mice on the main Antipodes altered ecosystem function (Eriksson and Eldridge Island, prior to their eradication in winter 2016 (Horn 2014). On subantarctic islands, mice consume most of et al. 2018). We combined invertebrate pitfall trapping the food items available (Le Roux et al. 2002). with stomach contents and stable isotope analyses to However, invertebrates are a favoured prey item, and determine: (1) what are the major resources for mice mice can contribute to their decline and even extinc- on Antipodes Island? (2) which invertebrates have tion (Rowe-Rowe et al. 1989; Le Roux et al. 2002; been most impacted by mice compared to uninvaded Smith et al. 2002). Through their predation of offshore islands? and (3) which invertebrates are invertebrates, mice may also compete with insectiv- preferentially targeted as prey? Together this allowed orous birds and impact on ecosystem function and us to make predictions about anticipated species trophic links (Huyser et al. 2000; Marris 2000;Le recoveries following mouse eradication. This work Roux et al. 2002; Miskelly et al. 2006). was undertaken over the course of three ﬁeld trips: The Antipodes Islands in the New Zealand sub- summer (January) 2011, winter (July) 2013, and antarctic region are remote, but mice have been autumn and winter (April to July) 2016. present as the sole invasive mammal since the early 1900s. Given their unique genetics in New Zealand, the founders are likely to have been from the Methods shipwreck of the President Felix Faure (Veale et al. 2018). Since colonisation, they have spread across the Study site entire main Antipodes Island, but have never been detected on nearby islands and rock stacks (Russell The Antipodes Islands (2097 ha; 49° 410 S; 178° 480 E) 2012). They were found to be ‘‘abundant at all lie 872 km south-east of New Zealand (Fig. 1). The altitudes’’ in 1969 (Warham and Johns 1975), but climate is characterised by strong south-westerly Marris (2000) noted that mouse abundance decreased winds with frequent cloud, fog and rain, and cool with increasing altitude. Density of mice on Antipodes temperatures (2–13 °C) with little seasonal variation Island was estimated at around 50–100/ha (Russell (Taylor 2006). The island group is an important and 2012; Elliot et al. 2015). Due to the unique ecosystem diverse breeding site for seabirds, and two species of and isolation of Antipodes Island, the impacts of mice endemic parakeets (Cyanoramphus spp.). Vegetation are concerning, particularly as endemic birds, inver- on the main Antipodes Island (2025 ha) is entirely tebrates and plants might constitute major prey items composed of tussock grassland (Poa and Carex spp.) (Moors and Atkinson 1984; Godley 1989; Patrick interspersed with some shrubs (Coprosma spp.) and 1994). ferns (see Godley 1989 for a complete description). 123 Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island 1267

178°45’E 178°48’E Archway Island ANTIPODES ISLANDS Locality Map N 0 500 North I km NEW ZEALAND 40 Bollons Island South I Chatham Is

Snares Is Bounty Is Antipodes Is Auckland Is 50 Campbell I

160 170 180

49°40’S Anchorage Bay

Hut Cove Reef Point Conical Hill 135 Stella Bay Orde Lees Islet North Plains Windward Islands Crater Bay 49°41’S

Alert Bay

366 Cave Point Mt. Galloway

am Central Plateau tre Southwest Dougall S Leeward Island Plain Mt. Waterhouse 49°42’S Stack Bay 356

Southern

Valley Ringdove

Stream Ringdove Bay

Bay Albatross Point h ut o S

0 1 2

Fig. 1 Antipodes Islands. Sampling sites are indicated by asterisks

Five study sites were focused upon. At the north-east locations with dense tussock vegetation reaching end of the island Anchorage Bay, Hut Creek and Reef 2 m in height; whereas the more distant higher altitude Point sites are neighbouring low altitude coastal North Plains plateau site supports lower vegetation of 123 1268 J. C. Russell et al.

0.5 m height made up of separated cushion plants vegetation, and unknown material were estimated (Russell 2012). The fifth study site was the summit of visually under a binocular microscope. Then the the highest point on the island, Mt Galloway. invertebrate portion was examined under a binocular microscope to determine the minimum number of Pitfall trapping representatives of each Order as calculated from identifiable remains. Identification was made through Surface invertebrates were pitfall trapped at Anchor- reference to invertebrate collections held at the age Bay, Reef Point, Hut Creek, the North Plains and University of Auckland and voucher specimens are the summit of Mt Galloway in summer (January) lodged at the Auckland War Memorial Museum. 2011, winter (July) 2013 and winter (June) 2016 and These data were used to determine mouse preference on the mouse-free offshore islands of Bollons and for different invertebrate Orders as reflected by Leeward in winter (July) 2016. At each site, ten pitfall proportional occurrence in their diet relative to traps (80 mm diameter, 90 mm depth) were spaced proportional abundance in pitfall traps on Antipodes 10 m apart. Traps were buried with their rim flush with Island in summer 2011 and winter 2016. the surface of the ground. They were then covered with a green plastic lid and filled to approximately Stable isotopes 2 cm depth with a 50/50 mix of glycol and water plus a drop of detergent. After at least 10 days (exactly in Samples for stable isotope analysis were collected in 2011 and 2013, but variable in 2016), the trap contents summer (January) 2011 and winter (July) 2013 at were removed and subsequently identified to Class or Anchorage Bay, Reef Point and North Plains, except Order, except for Coleoptera (beetles), which were for land and seabird samples, which were collected at identified to species. These data were used to deter- large across the island. Mice were live-captured in mine baseline impacts of the presence of mice on Longworth traps baited with peanut butter, euthanised, invertebrate relative abundance, by comparing relative and liver samples were taken during autopsy. Land abundance on the mouse-invaded main Antipodes birds were captured in nets and seabirds by hand, and Island with mouse-free offshore islands of Bollons and all were bled from the metatarsal vein. Land inverte- Leeward in winter 2016. The effects of site, nested brates were pitfall trapped or litter sorted and identi- within mouse status, on invertebrate communities fied to Order. These samples were collected in were tested using permutation multivariate analyses of association with other population biology (see Russell variance with 999 permutations, and visualised with 2012) and non-target impact assessment work being non-metric multidimensional scaling using Euclidean undertaken on Antipodes Island in preparation for distance. Euclidean distance was used instead of a mouse eradication. Marine invertebrates, land plants species similarity measure because the islands share and marine macroalgae were all hand-collected. All the same pool of invertebrate species and the focus tissue samples were stored at room temperature in the was on changes in their abundance and distribution. same batch of 70% ethanol, with the exception of feathers that were stored dry and loose in bags. These Stomach contents samples were used to determine mouse preference for resources other than invertebrates on Antipodes Twenty mice were captured using Victor snap-traps Island. baited with peanut butter placed at Anchorage Bay, Samples (excluding blood) were cleaned, dried, Reef Point and the North Plains in summer (January) ground and weighed to the nearest microgram. Soft- 2011 and at Hut Creek in autumn (April) 2016. The body tissue was first removed from hard-shelled contents of mouse stomachs were individually sieved organisms (snails and limpets). Lipids were not (1 mm2) under running water and emptied into Petri extracted from animal specimens, but d13C values dishes for examination. All stomachs examined were were corrected following equations in Fry (2002). over one quarter full and so should not over-represent Stable isotope analyses were carried out on a DELTA hard parts of prey as per Le Roux et al. (2002). V Plus continuous flow isotope ratio mass spectrom- Stomach contents were quantified in two ways. The eter linked to a Flash 2000 elemental analyser using a volume of invertebrate and vertebrate remains, MAS 200 R autosampler (ThermoFisher Scientific, 123 Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island 1269

Bremen, Germany) at the NIWA Environmental (Barrow et al. 2008; Bugoni et al. 2008; Kiszka et al. Stable Isotope Facility in Wellington, New Zealand. 2014; Hogsden and McHugh 2017). Regardless, the Using ISODAT (Thermo Fisher Scientiﬁc) software, use of the same solvent for all samples from these 15 d N values were calibrated against a N2 reference within-year analyses will further reduce any errors of gas. Carbon isotope values were calibrated against a interpretation that may be associated with its use.

CO2 reference gas, relative to the international stan- Similarly, although samples were obtained from dard Carrara Marble NSB-19 (National Institute of different tissue types for different taxa, differential Standards and Technology (NIST), Gaithersberg, MD, fractionation was also assumed to have minimal effect USA). NSB-19, was calibrated against the original Pee on stable isotope values, so no correction factor was Dee Belemnite (PDB) limestone standard and was applied during the modelling analysis. All analyses then corrected for 17O. Sample d15N values were two- were undertaken in R 3.4.3. point normalised using isotopic data from the daily analysis of National Institute of Standards and Tech- nology (NIST) 8573 USGS40 L-glutamic acid and Results NIST 8548 IAEA-N2 Ammonium sulphate. Sample d13C values were two-point normalised using isotopic Pitfall trapping data from the daily analysis of NIST 8573 USGS40 L- glutamic acid and NIST 8542 IAEA-CH-6 Sucrose. Results from invertebrate pitfall trapping on the main Estimates of precision were obtained from repeat Antipodes Island in summer (January) 2011 and analysis of the working laboratory standard DL- winter (July) 2013 have been described elsewhere Leucine (DL-2-Amino-4-methylpentanoic acid, (Russell 2012; Elliot et al. 2015). We present the C6H13NO2, Lot 127H1084, Sigma, Australia) which additional pitfall trapping results, collected in associ- gave a precision better than 0.15% (1 SD) for both ation with mouse eradication on the main Antipodes carbon and nitrogen. Data from the daily analysis of Island, and for the first time, mouse-free offshore USGS65 Glycine were used to check accuracy, with islands from winter (June) 2016. both carbon and nitrogen accurate to within 0.2% over On the main Antipodes Island in winter 2016, the analysis period of a year. similar to winter 2013, most invertebrates collected Univariate analyses of variances were used to were Coleoptera (36%) followed by Isopoda (26%) identify significant differences in stable isotope values and Diptera (21%). Over one-third of the individuals among taxonomic groups and years (as a proxy for were collected at Anchorage Bay (35%), where pitfall seasons). The contribution of each potential source to traps were out for the standard length of 10 nights, mouse diet, considered separately by year, was then followed by North Plains (27%), Reef Point (20%) and determined using Bayesian mixing models imple- Hut Creek (10%) where pitfall traps were out for a mented in the R package SIMMR (Parnell et al. 2013). longer period of 15 nights. In contrast, on the mouse- Trophic discrimination factors for mouse livers were free offshore islands in winter 2016, where pitfall traps obtained through taking the mean and standard were out for 13 nights, most invertebrates collected deviation from the values reported from studies on were Coleoptera (49%) followed by Amphipoda this specific tissue in the literature (DeNiro and (44%). For all taxa combined more individuals were Epstein 1978, 1981; Arneson and MacAvoy 2005). collected on Bollons Island (71%) compared to Although obtaining trophic discrimination factors Leeward Island (29%). from controlled feeding studies would be optimal, in Differences in invertebrate communities among this case it was not logistically practical. Samples were islands and sites were primarily driven by the presence only compared within a year, where all samples were of mice on the main Antipodes Island (R2 = 0.56, preserved in the same ethanol batch. Such storage was p \ 0.001) and then among sampling sites on the main necessary given the remote location of the study site. Antipodes Island (R2 = 0.22, p \ 0.001). A non- While there is debate within the literature, this storage metric multidimensional scaling has low stress method has been shown to have minimal effect on (0.03) and clearly shows the separation among islands stable isotope ratios of nitrogen or carbon in relevant with and without mice, and the greater variation in taxa including invertebrates, birds and mammals abundances of invertebrates on the latter (Fig. 2). 123 1270 J. C. Russell et al.

Amphipoda Isopoda Oligochaeta

Hemiptera PseudoscorpionidaHymenoptera Gastropoda Araneae NMDS2

Neuroptera Coleoptera Lepidoptera Diptera

Anchorage Bay Reef Point Chilopoda Hut Creek North Plains Mt Galloway Leeward I. Bollons I. −150 −100 −50 0 50 100 150

−150 −100 −50 0 50 100 150 NMDS1

Fig. 2 Non-metric multidimensional scaling (NMDS) bi-plot offshore Leeward and Bollons Islands (grey). Different sam- of invertebrate communities comprising 14 Orders on the pling sites are indicated by symbols as shown in the mouse-invaded main Antipodes Island (black) and mouse-free ﬁgure legend. Stress = 0.03 For all taxa combined in 2016, average invertebrate Lepidoptera, 238% in Diptera and 873% in abundance in pitfall traps on mouse-invaded Anti- Gastropoda. podes Island was 15% of the invertebrate abundance of pitfall traps on mouse-free offshore islands, even Stomach contents though pitfall traps were out for a shorter time at most of the latter sites. While the number of Orders detected Mouse stomachs contained invertebrate remains, plant between invaded and uninvaded islands was similar, material (leaf, seed and stem fragments), and bird abundance responses were variable with reductions of remains (feathers, fat deposits, skin and muscle) 100% in Amphipoda, 89% in Chilopoda and Coleop- (Table 1). All stomachs that had vertebrate remains tera and 62% in Aranae, but increases of 20% in also contained feathers. The nine mouse stomachs

Table 1 Frequency of Food category occurrence and volume of each dietary component for Invertebrate Vertebrate Vegetation Unknown mice caught on Antipodes Island in summer (January) January 2011 2011 and autumn (April) Frequency of occurrence (n =9) 9 4 8 6 2016 Percentage range 90–95 0–5 0–10 0–10 April 2016 Frequency of occurrence (n = 11) 9 9 11 9 Percentage range 0–80 0–75 1–95 0–30

123 Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island 1271 collected in summer (January) 2011 generally had components being Diptera larvae (41% of the identi- much higher volumes of invertebrate remains com- ﬁed individuals), Lepidoptera larvae (26%), Acarina pared to the 11 collected in autumn (April) 2016 (13%), adult Coleoptera (8%) and Araneae (7%). (mean ± SE: 21 ± 11 vs. 3 ± 1 minimum inverte- Diptera larvae and Acarina were only present in two brate individuals). Higher levels of bird remains and mouse stomachs (M32 and M34) from mice caught at plant material were seen in the autumn compared to the Anchorage Bay penguin colony (Table 2). The summer samples (Table 1). Acarina observed are most likely the species, Ixodes Overall eight invertebrate Orders were identiﬁed in uriae, as noted by Marris (2000). Three individuals of stomachs (Table 2) with the most common the endemic weevil, Gromilus insularis antipodarum,

Table 2 Minimum number of invertebrates per Order and occurrence of feathers in 20 mouse stomachs from Antipodes Island Minimum number of individuals Stomach ID M31 M32 M34 M129 M130 M132 M133 M134 M173 M801 Location RP AB AB NP NP NP NP NP NP HC

Aves Feathers present No Yes Yes No No Yes No Yes No No Arachnida Acarina 0 22 6 0 0 0 0 0 0 0 Araneae 1 1 1 1 0 1 1 2 1 0 Insecta Coleoptera (larvae) 0 0 0 0 0 0 0 1 0 0 Coloeptera (adult) 1 2 0 2 1 2 1 3 3 0 Diptera (larvae) 0 80 9 0 0 0 0 0 0 0 Lepidoptera (larvae) 1 0 10 7 1 17 1 5 1 0 Lepidoptera (adult) 0 0 0 0 0 0 0 0 0 0 Thysanoptera 0 0 0 0 0 0 0 0 0 0 Oligochaeta 0 0 0 1 0 0 0 1 0 0 Pseudoscorpionida 0 0 0 0 0 0 0 0 0 0 Stomach ID M803 M806 M855 M857 M859 M860 M861 M863 M866 M880 Location HC HC HC HC HC HC HC HC HC HC

Aves Feathers present Yes No Yes Yes Yes Yes Yes Yes Yes Yes Arachnida Acarina 0000000000 Araneae 1121001100 Insecta Coleoptera (larvae) 0101000000 Coloeptera (adult) 0010001000 Diptera (larvae) 0000000000 Lepidoptera (larvae) 1226010100 Lepidoptera (adult) 0010000000 Thysanoptera 0000000010 Oligochaeta 0100000000 Pseudoscorpionida 0000000010 Trapping locations: RP = Reef Point, AB = Anchorage Bay, NP = North Plains crater (all summer 2011), HC = Hut Creek (autumn 2016) 123 1272 J. C. Russell et al. were identified from one stomach (M173). Oligo- traps for which they are not susceptible or mouse chaeta, Coleoptera larvae, adult Lepidoptera, Pseu- stomachs most likely because they are scarce in the doscorpionida and Thysanoptera were also identified. ecosystem as a preferred diet item of mice. Mice stomach contents analysis suggested that The isotopic niches of terrestrial sources were Orders such as Diptera larvae were being opportunis- tightly circumscribed and overlapping (Fig. 4). Iso- tically consumed (low incidence prey items but topic niches differed little between years except in consumed in high proportions when encountered) d15N values where land bird nitrogen isotope values while others such as Araneae, Coleoptera adults and increased in winter (p = 0.01), while mice decreased Lepidoptera larvae were regularly consumed staple in winter (p \ 0.01). Results from the SIMMR mixing diet items (all high incidence prey items) (Fig. 3). model indicated that mouse diets varied between Mice were differentially targeting some Orders of seasons, being dominated by invertebrates and land invertebrates relative to their abundance in pitfall traps birds in summer 2011 (63% of diet), with a greater on the main Antipodes Island. In both summer 2011 reliance on plants and seabirds in winter 2013 (72% of and winter 2016, Lepidoptera were preferentially diet) (Table 4, Fig. 5). Marine macroalgae are also targeted by over 200-fold and Oligochaeta over likely to increase in importance during the winter. 20-fold, while Coleoptera at only 0.26–0.39 of their However, as a result of isotopic overlap among relative abundance. sources (Fig. 4), model outputs struggled to resolve estimates between some potential sources, and this Stable isotopes issue is reflected in the wide credible intervals for land bird consumption in summer 2011 (high negative A total of 398 samples for stable isotope analysis were correlation with land invertebrates, - 0.94) and obtained from across the main Antipodes Island seabirds in 2013 (strong negative correlations with (Table 3). Unfortunately, some key taxa (e.g. adult both land plants, - 0.80, and marine macroalgae, Lepidoptera) were not available from either pitfall - 0.75).

Fig. 3 Incidence versus proportion of invertebrates per order of food items in 20 mouse stomachs from Diptera Antipodes Island (larvae)

Lepidoptera (larvae) Proportion

Acarina Coleoptera (adult) Araneae

Coleoptera Lepidoptera (larvae) (adult)

0.0 0.1Oligochaeta 0.2 0.3 0.4 0.5 Thysanoptera Pseudoscorpionida

0 5 10 15 Incidence

123 Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island 1273

Table 3 Samples for Organism Tissue 2011 2013 d15N d13C table isotope analysis collected on Antipodes Land mammals 15.37 (3.10) - 23.76 (4.08) Island in summer (January) Mice Liver 63 64 2011 and winter (July) 2013 Land birds 12.17 (4.39) - 21.08 (3.23) Antipodes parakeet Blood 5 5 Reischeks parakeet Blood 5 5 Antipodes snipe Blood 5 5 Antipodes pipit Blood 5 5 Seabirds 11.89 (4.20) - 21.15 (2.99) White-headed petrel Blood 5 – White-chinned petrel Blood 5 1 Grey-backed storm petrel Blood 5 1 Light-mantled sooty albatross Blood 2 – Erect crested penguin Feather 5 – Rock hopper penguin Feather 4 – Soft-plumaged petrel Blood 5 – Fairy prion Blood 5 – Northern giant petrel Blood 5 – Subantarctic skua Blood 3 – Antipodean albatross Blood 5 5 Grey petrel Blood 1 5 Land invertebrates 14.15 (3.92) - 22.45 (4.39) Coleoptera Body 5 4 Isopoda Body 6 5 Araneae Body 5 4 Diptera Body 5 4 Gastropoda Body (no shell) 2 1 Marine invertebrates 13.83 (4.10) - 22.36 (4.59) Cellana strigilis Body (no shell) 4 5 Land plants 13.73 (4.25) - 23.64 (4.60) Anisotome antipoda Seed/Foliage 7 7 Poa litorosa Seed/Foliage 7 7 Carex triﬁda Seed/Foliage 5 6 Leptinella plumosa Foliage 5 5 Crassula moschata Foliage 4 4 Urtica australis Seed/Foliage 5 4 Carex appresa Seed/Foliage 5 5 Coprosma perpusilla Fruit/Foliage 6 6 Coprosma ciliata Foliage 5 4 Marine macroalgae 13.48 (4.20) - 23.09 (4.73) Durvillaea antarctica Foliage 5 5 Mean (SD) are given for Gigartina pachymenioides Foliage 5 5 each taxonomic group

Discussion that at high latitudes mouse diet is dominated by invertebrates (St Clair 2011). Pitfall trapping of The majority of food items identiﬁed in stomachs were invertebrates showed a severe reduction in abundance, invertebrate fragments, consistent with global ﬁndings but not in diversity, attributable to mice on the main 123 1274 J. C. Russell et al.

Summer 2011 Winter 2013

mice land invertebrates 25 land birds marine invertebrates 20 marine macroalgae land plants seabirds 20 d15N d15N

10 10 −30 −20 −10 −30 −25 −20 −15 −10 d13C d13C

Fig. 4 d15N and d13C values of mice on Antipodes Island in summer (January) 2011 and winter (July) 2013. Resources are shown as mean ± SD

Table 4 Dietary proportions of mice on Antipodes Island in component of stomach contents, as found on other summer (January) 2011 and winter (July) 2013 estimated from subantarctic islands (Copson 1986; Crafford and SIMMR mixing model Scholtz 1987; Rowe–Rowe et al. 1989; Le Roux Year 2011 (summer) 2013 (winter) et al. 2002; Smith et al. 2002). Such strong preference Source Mean SD Mean SD for certain prey items suggests that mice are systematically consuming their way through the terrestrial Land birds 0.354 0.243 0.032 0.027 ecosystem by exhausting preferred prey and then Seabirds 0.115 0.087 0.287 0.150 moving on to the next preferred prey source. The end Land invertebrates 0.274 0.144 0.038 0.027 point of this may be similar to that observed on other Marine invertebrates 0.081 0.047 0.033 0.022 subantarctic islands where diet shifting from lower Land plants 0.119 0.074 0.437 0.088 trophic levels to large seabirds eventually occurs Marine macroalgae 0.057 0.032 0.172 0.078 (Cuthbert et al. 2013, 2014; Dilley et al. 2018; McClelland et al. 2018). This is potentially an outcome of mice, having been present for much longer Antipodes Island compared to mouse-free offshore on those islands, exhausting all other available food islands. This difference was driven by certain taxa, resources. which are presumably differentially preyed upon. Mice have previously been invoked as the driver for Amphipoda, in particular, dominated pitfall traps on a cessation in snipe (Coenocorypha aucklandica mouse-free offshore islands, but were virtually absent meinertzhagenae) breeding activity over summer, on the mouse-invaded main island. Comparison of through an unknown mechanism that is only observed mouse stomach contents to prey availability suggested on Antipodes Island (Miskelly et al. 2006). Our results ongoing prey preference by mice for some remaining found that over summer land birds do indeed feed taxa on Antipodes Island. In particular, we found signiﬁcantly lower in the food chain, putatively an Lepidoptera larvae to be a relatively common outcome of competition with mice for invertebrates,

123 Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island 1275

Fig. 5 Comparison among Summer 2011 Winter 2013 estimated proportions of mouse diet on Antipodes Island in summer (January) seabirds 2011 and winter (July) 2013 using SIMMR source land plants apportionment model. Boxes comprise 25–75% credible intervals and marine macroalgae whiskers illustrate 95% credible intervals Source marine invertebrates

land birds

land invertebrates

0.00 0.25 0.50 0.75 0.00 0.25 0.50 0.75 Proportion Proportion which may prevent snipe reaching adequate breeding detect via traditional stomach contents analysis, and condition. Furthermore, mice may also prey upon land stable isotopic mixing models do suggest that verte- birds over summer. This suggests that mice do indeed brate consumption has the potential to be higher than have a strong impact on snipe through exploitation recorded via traditional methods. However, the high competition, and potentially also predation. Early negative correlation between land bird and land monitoring of terrestrial ecosystem recovery follow- invertebrate sources in summer means that estimated ing the eradication of mice on Antipodes Island has proportions consumed for these two sources are poorly already reported a fivefold increase in snipe detection resolved (Parnell et al. 2013; Brett 2014). Thus, (Cox 2018). combining information from both methods suggests While feathers were found in a high proportion of that land invertebrates are the key resource for mice on mouse stomachs, scavenging is considered the most Antipodes Island, and that while land birds are also likely source of vertebrate material in the mouse diet. likely to be consumed, the proportion may well be The two stomachs from the Anchorage Bay penguin lower than the mean credible interval suggests. colony contained feathers, Dipteran larvae, and Similarly, mixing models also struggled to resolve Acarina of a size consistent with being ecto-parasites dietary proportions between the three most highly of a large bird, suggesting that a rotting bird carcass consumed sources in winter. The isotopic niches of was scavenged with the ecto-parasites and maggots taxonomic groups living in the terrestrial ecosystem of also consumed. Mice are adept scavengers and Antipodes Island were heavily overlapping, reflecting consuming a bird carcass would also result in feathers the limited resource base found on the isolated island being ingested (e.g. Smith et al. 2002). Bird carcasses group, with notable subsidy by marine resources on Antipodes Island are cleaned to the bone in a matter (Anderson and Polis 1998). Such overlap can be of days (JCR pers. obs.). However, we cannot rule out problematic when trying to resolve consumer diet predation, particularly on nestlings of small land and source using stable isotopes and can bias towards sea birds, and mice on Antipodes Island have been generalist solutions (Brett 2014). However, the pat- hypothesised to prey upon storm petrels (Moors and terns we found were qualitatively consistent between Atkinson 1984; Angel et al. 2009). Regardless, both stomach contents and stable isotopes, and similar forms of consumption will alter the nutrient flow on seasonal shifts have been found on other subantarctic Antipodes Island (Drake et al. 2011). islands (e.g. Le Roux et al. 2002; Smith et al. 2002). Consumption of resources such as eggs and soft To determine the impacts of mice on Antipodes bird and invertebrate tissues would be difficult to Island we made a number of assumptions. In

123 1276 J. C. Russell et al. particular, we assumed that any differences in inver- and land birds over summer to terrestrial vegetation tebrate diversity between mouse invaded and unin- and seabirds in winter. Combining multiple method- vaded islands were only attributable to mice, and not ological approaches to examine the diet of this other variables which we blocked for within our study invasive species has allowed us to robustly estimate design (e.g. season and habitat) and that our pitfall these effects. Stable isotopes have been proposed as a traps randomly sampled the landscape and available tool to rapidly detect ecosystem recovery following prey items. Although pitfall traps can be biased in the invasive rodent eradication (Nigro et al. 2017). types of invertebrates they capture, they are likely a However, due to the limited and isotopically similar good characterisation of medium and large sized prey base on Antipodes Island, this method would surface macroinvertebrates, which would be the struggle to capture changes in native consumers if preferred prey of mice (Chown and Smith 1993). used in isolation. Changes in native avian species Our sample size for stomach contents was also following eradication are more likely to be numerical necessarily small as it had to make use of available in response to increased prey abundance, rather than material collected pre-eradication. However, Le Roux being reflected in substantial changes in niche breadth et al. (2002) found that analysing five to nine mouse or prey type, unless functional responses also change stomachs from Guillou Island represented 90% of the with prey abundance. By combining stable isotopes principal contents of the 212 stomachs collected. Our with classical stomach contents analysis and prey comparison between seasons is problematically con- availability comparisons between mouse-invaded and founded by year. However, annual climate cycles on uninvaded islands, we were able to reliably demon- islands in the Southern Ocean are strong and consis- strate that systematic invertebrate prey preference by tent, compared to tropical islands (Russell and Holmes invasive mice on the main Antipodes Island was 2015), and inferred temperature records (Leihy et al. occurring. This was directly impacting some inverte- 2018) showed that neither 2011 nor 2013 were brate Orders and indirectly impacting competing avian anomalous years. consumers on the island. These wide-ranging impacts Based on our study, we would expect to see further suggest that eradication of mice from Anti- substantial increases in the abundance of snipe, and podes Island will release native species from both invertebrate Orders including Amphipoda and Lepi- competitive and predatory effects, with consequent doptera, following eradication of mice. Additional changes to nutrient flow in this isolated ecosystem. complex changes will also occur within taxa (e.g. Samaniego-Herrera et al. 2017). For example, pre- Acknowledgements For assistance collecting samples in the ferred Coleoptera species (e.g. three specimens of the field the authors thank David Thompson, Erica Sommer, David Boyle and Mark Fraser in summer 2011, Helen Nathan, Terry rare endemic Antipodes Islands weevil sub-species Greene and Graeme Elliott in winter 2013, Fin Cox in autumn Gromilus insularis antipodarum were found in one 2016 and Jose Luis Herrera in winter 2016. Thanks to the stomach) have been extirpated or severely reduced on Department of Conservation, Murihiku, for logistical support, the main Antipodes Island. However, those Coleoptera and Hank Haazen and crew of the Tiama for transport. Funding was provided for the summer 2011 expedition by NIWA and species that remain are now a less preferred prey item winter 2013 expedition by the National Geographic Society (e.g. the abundant Stenomalium n.sp.). This leads to (Grant No. 9322-13). Thanks to Stephen Thorpe, Robert Hoare, the counter-intuitive result of Coleoptera as a group and John Marris for taxonomic identification of invertebrate being less abundant on the main Antipodes Island, samples. Thanks to Surrya Khanam for laboratory sorting, Julie Brown and Anna Kilimnik for stable isotope laboratory analyses while at the same time no longer being a preferred prey and Wendy Nelson for macroalgae identification. JCR is item due to species composition. Furthermore, feed- currently funded by the Royal Society of New Zealand backs among taxa may alter recoveries e.g. inverte- Rutherford Discovery Fellowship (Grant No. RDF- brate recovery may be dampened if land birds UOA1404). TWB is currently funded by the European Union’s Horizon 2020 research and innovation programme recovering from predation exert top-down limitation Marie Skłodowska-Curie Fellowship (Grant No. 747120). upon them (Sinclair et al. 2005). Thanks to Katherine Russell and two anonymous reviewers Our study suggested broad predatory and some for feedback on the manuscript. This research was conducted competitive impacts of mice across the terrestrial under DOC entry (SO-29716-LND 1011/35) and research (SO- 29140-FAU 1011/20) permits, and University of Auckland ecosystem. These impacts varied with seasons, track- Animal Ethics Committee approval (R845). ing resource availability from abundant invertebrates 123 Systematic prey preference by introduced mice exhausts the ecosystem on Antipodes Island 1277

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